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Staying Well Connected – Lithistid Sponges on Seamounts Merrick Ekins1, Dirk Erpenbeck2, Gert Wo¤Rheide3 and John N

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Staying Well Connected – Lithistid Sponges on Seamounts Merrick Ekins1, Dirk Erpenbeck2, Gert Wo¤Rheide3 and John N Journal of the Marine Biological Association of the United Kingdom, 2016, 96(2), 437–451. # Marine Biological Association of the United Kingdom, 2015 doi:10.1017/S0025315415000831 Staying well connected – Lithistid sponges on seamounts merrick ekins1, dirk erpenbeck2, gert wo¤rheide3 and john n. a. hooper1,4 1Queensland Museum, PO Box 3300, South Brisbane 4101, Brisbane, Queensland, Australia, 2Department of Earth and Environmental Sciences and GeoBio-Center, Ludwig-Maximilians-Universita¨tMu¨nchen, Richard-Wagner-Straße 10, 80333 Mu¨nchen, Germany, 3SNSB – Bavarian State Collections for Palaeontology and Geology, Richard-Wagner-Straße 10, 80333 Mu¨nchen, Germany, 4Eskitis Institute for Drug Discovery, Griffith University, Brisbane 4111, Queensland, Australia Three species of lithistid sponges, Neoaulaxinia zingiberadix, Isabella mirabilis and Neoschrammeniella fulvodesmus were collected from deep seamounts off New Caledonia to address questions about their population structure, gene flow and the relative contribution of sexual and asexual reproductive strategies to their populations. The sponges were tested by sequencing the ITS (internal transcribed spacer) and CO1 regions of their genomes. These rare and presumably ancient sponges have a distribution restricted to seamounts in the south-western Pacific. Deep seamounts represent geographically separated islands. Although the sponges could be expected to have sexual reproduction restricted to near neighbours due to low sexual dispersal opportunities via larvae, this study found surprisingly high levels of gene flow between the seamounts. Amongst the specimens of N. zingiberadix taken from two seamounts there was no population structure; CO1 resulted in identical genotypes. For the population structure within N. fulvodesmus, as revealed by ITS, most of the variation was within each individual from the six seamounts on which it occurred and CO1 revealed no difference between individuals or seamounts. The third species I. mir- abilis showed four genotypes based on CO1, which were distributed across all the seamounts. Indirect measures of different species showed a range of reproductive strategies from asexual to sexual, but with much higher connection between seamounts than previously thought. Individual seamounts did not show a separate population structure as one might expect from ‘islands’. The conclusion must be that these sponges have mechanisms to attain greater dispersal than previously thought. Keywords: Lithistid, population genetics, seamounts, gene flow, dispersal, reproduction, Neoaulaxinia zingiberadix, Isabella mirabilis, Neoschrammeniella fulvodesmus Submitted 23 January 2015; accepted 19 May 2015; first published online 22 June 2015 INTRODUCTION transmission of a sexual form, such as detached tissue still undergoing post fertilization development (Maldonado & Sponges occupy widely divergent biogeographic regions. This Uriz, 1999b), sperm and eggs, or a swimming or crawling may be a testament to their ability to colonize over long dis- larval stage that lasts for only a few days (Maldonado & tances, or their ability to adapt and evolve to suit changing Riesgo, 2008). These are potentially transmitted via currents, environments. Yet the mechanisms whereby they do this, in waves, storms or using vectors such as fish or echinoderms. particular the relative importance of both sexual and asexual Asexual reproduction has also been observed and includes reproduction strategies, is largely unknown for many abiotic factors such as physical fragmentation (Wulff, 1991) sponges. Sponges found on seamounts are isolated, sub- and biotic factors such as fission, budding (e.g. Teixido merged and independent offering an opportunity to test et al., 2006; Ereskovsky & Tokina, 2007) and gemmule forma- various possibilities. tion (Sara` et al., 2002). Both strategies have been shown to Sponges are known to use both sexual and asexual repro- occur in individual sponges concurrently (Leong & Pawlik, ductive strategies to survive and prosper (Kaye, 1990) and 2010) or successionally (Ereskovsky & Tokina, 2007). It is both sexual and asexual components to enable long-range dis- the sponges’ ability to use both of these strategies synergistic- persal and colonization of new habitats (see overview in ally, that improves their dispersal ability (Maldonado & Uriz, Maldonado & Riesgo, 2008). Active locomotion of entire indi- 1999a). The formation of external buds of hexactinellids in the vidual sponges has been observed in response to environmen- stable environment of Antarctic waters (Teixido et al., 2006) tal factors (Bond & Harris, 1988; Maldonado & Uriz, 1999b), may enable the formation of a stable clonal population in but such an ability, used to readjust the sponge position at the the immediate vicinity. The formation of gemmules generally microhabitat scale (displacements from millimetres to centi- associated with freshwater sponges also occur in some marine metres) cannot account for population dispersal. Dispersal sponges (Sara` et al., 2002). However, these gemmules are of sexual stages is generally assumed to involve the expected to have dispersal abilities on par with sexual propa- gules. The formation of bubble-like buds in Oscarella spp. (Ereskovsky & Tokina, 2007) and Leucetta changosensis Corresponding author: Dendy, 1913 (Wo¨rheide et al., 2008) shows a previously M. Ekins unnoticed far-reaching asexual dispersal mechanism. Email: [email protected] Merging of conspecific sponges (Wulff, 1990) also provides 437 Downloaded from https://www.cambridge.org/core. UB der LMU München, on 03 Dec 2018 at 14:12:47, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0025315415000831 438 merrick ekins et al. another possible asexual reproduction mechanism which is Population research in sponges has largely concentrated on not usually accompanied by meiotic recombination but biogeography (Nichols & Barnes, 2005), the movement of carried out by totipotent somatic cells in sponges. species into or out of the Mediterranean Sea (Duran et al., Colonization of new locations by asexual stages may, 2004a), survival in the South Pacific (Wo¨rheide et al., alternatively, be more commonly due to the dispersal of frag- 2002a) and ecological specialization (Duran & Ru¨tzler, ments or entire sponges, via waves, currents, storms and 2006). Much of the work on sponge population genetics has cyclones, or as a passenger on substrates such as debris. shown genetic differentiation at geographic scales (Klautau There are several characteristics that may indicate an et al., 1999; Duran et al., 2004a, b; Bentlage & Worheide, asexual or clonal population including frequent recovery of 2007; Hoshino et al., 2008;Wo¨rheide et al., 2008; Xavier genotypes, correlation between different independent et al., 2010); for a review see Uriz & Turon (2012). By com- markers, linkage disequilibrium and the absence of sexual parison, only a small amount of research has been carried reproductive structures. Direct observation of deep sea out on small scales as would occur on a seamount. Two sponge dispersal is not currently feasible, although observa- Mediterranean studies on Crambe crambe (Schmidt, 1862) tions indicate it can be done at great expense (Teixido et al., (Calderon et al., 2007) and Scopalina lophyropoda Schmidt, 2006). In other sessile invertebrates such as corals, asexual 1862 (Blanquer et al., 2009) showed genetic structure at this reproduction is common and is an adaptation that succeeds small scale consistent with what one would expect from a both in moderate to high levels of disturbance (Le Goff- poorly dispersing sexual stage, although this result could be Vitry et al., 2004; Miller & Ayre, 2004) and stable environ- confused by the presence of chimeric individuals (Blanquer ments (Foster et al., 2007) as it enables well-adapted & Uriz, 2011). Seamounts have been predicted to have large individuals (Ayre & Willis, 1988) to rapidly colonize environ- amounts of population structure because of spatial separation ments or maintain dominance in environments unfavourable and limited dispersal mechanisms coupled with high levels of for sexual reproduction (Wulff, 1991; Hughes et al., 1992). asexual reproduction (Richer de Forges et al., 2000; Samadi Branching corals, which have relatively fragile morphology, et al., 2006). Seamounts are believed to be particularly suscep- are more likely to have high asexual components tible to genetic drift due to their small size (Le Goff-Vitry et al., (Le Goff-Vitry et al., 2004) than more stable massive corals 2004). Seamounts are not ephemeral and, coupled with low (Foster et al., 2007). By contrast, the coral excavating sponge gene flow due to distance and hydraulics, structure within Cliona delitrix Pang, 1973 was shown to not have clonal populations would be expected (Samadi et al., 2006). propagation, as was expected, resulting from coral breakage However, research on crustaceans collected from New (Zilberberg et al., 2006b). Caledonian seamounts showed that previous perceived high Research has been carried out exploring the contributions endemism (Richer de Forges et al., 2000) was not the case of sexual and asexual recruitment on sponges from physical for seamounts. Instead the crustaceans had high levels of observations (Battershill & Bergquist, 1990; Wulff, 1991). gene flow between the seamounts. The only exception in However, other indirect methods to assess the relative input fact was a gastropod that
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